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Hair Testosterone and Cortisol Concentrations in Pre- and Post-Rut Roe Deer Bucks: Correlations with Blood Levels and Testicular Morphometric Parameters

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Hair Testosterone and Cortisol Concentrations in Pre- and Post-Rut Roe Deer Bucks: Correlations with Blood Levels and Testicular Morphometric Parameters animals Article Hair Testosterone and Cortisol Concentrations in Pre- and Post-Rut Roe Deer Bucks: Correlations with Blood Levels and Testicular Morphometric Parameters Domenico Ventrella ID , Alberto Elmi * ID , Francesca Barone, Giacomo Carnevali, Nadia Govoni ID and Maria Laura Bacci Department of Veterinary Medical Sciences, University of Bologna, 40064 Ozzano dell’Emilia (BO), Italy; [email protected] (D.V.); [email protected] (F.B.); [email protected] (G.C.); [email protected] (N.G.); [email protected] (M.L.B.) * Correspondence: [email protected]; Tel.: +39-051-209-7923 Received: 25 May 2018; Accepted: 3 July 2018; Published: 6 July 2018 Simple Summary: The roe deer is a very common wild species in Italy and shows peculiar reproductive characteristics. Sexually-mature males, called bucks, show a complete interruption in spermatogenesis during the cold seasons. The mechanisms behind such interruption are still partially unknown. Hair is a good biological sample, easy to obtain while minimizing stress, for endocrinological analyses that may provide information regarding such mechanisms. The aim of the work was to quantify and compare hair concentrations of testosterone and cortisol in wild roe deer bucks hunted during the pre- and post-rut period (mating season). The secondary objective was the evaluation of possible correlations of such hair concentrations with blood and morphometric parameters of the testes. Testosterone significantly increased from the pre- to post-rut period, while cortisol significantly decreased. The correlations with blood and testicular parameters resemble what is already described in the literature. Overall, this study represents a first report of the quantification of testosterone and cortisol in roe deer hair, and may provide interesting insights into their reproductive physiology. Abstract: The roe deer is a seasonally breeding species with a reproductive cycle regulated by endogenous rhythms and photoperiod-sensitivity. Sexually mature bucks show hormonal and testicular activation during the reproductive season, with a peak in the rut period, and following gradual involution. Hair is a good matrix for non-invasive endocrinological analyses that provide long-term information without being influenced by the hormones’ pulsating release patterns in blood. The aim of the work was to quantify hair concentrations of testosterone and cortisol in wild roe deer bucks hunted during the pre- and post-rut period, using a radioimmunoassay methodology, and to look for differences between the two periods. The secondary objective was the evaluation of possible correlations of such hair concentrations with blood and morphometric parameters of the testes. Both hormones showed statistical differences, with opposing trends, when comparing the two periods: testosterone increased while cortisol decreased. The correlation analysis was in agreement with existing literature regarding metabolism/actions of these hormones and testicular morphometric parameters. This study represents the first report of the use of radioimmunoassay techniques to quantify testosterone and cortisol in roe deer hair, and may provide interesting insights into their reproductive physiology. Keywords: roe deer; hair testosterone; hair cortisol; testicular morphometric parameters; reproductive physiology; radioimmunoassay Animals 2018, 8, 113; doi:10.3390/ani8070113 www.mdpi.com/journal/animals Animals 2018, 8, 113 2 of 9 1. Introduction Mammalian species living in the Northern hemisphere have developed different strategies in order to ensure successful breeding as an adaptation to the cycling environmental conditions of their habitats [1]. A good example of this adaptive process can be found in the seasonal reproductive cycle of the roe deer (Capreolus capreolus L., 1758), a European wild ruminant. Its reproductive season is characterized by three periods: pre-rut (mid-May/mid-July), rut (mid-July/mid-August) and post-rut (mid-August/September) [2], and is regulated by endogenous rhythms and high sensitivity to photoperiod [1]. Right before the pre-rut period (from the beginning of April), bucks show aggressive behaviors as they fight each other in order to establish hierarchy and territoriality [3]. In the same period, the first of the two annual sheddings takes place, with the complete substitution of the winter coat [4]. Once sexually mature, bucks show highly synchronized testicular cycles including transitions from totally arrested to highly activated spermatogenesis [5]. Spermatogenesis is directly linked to growth and involution patterns of the testicular mass [6]; indeed, during the rut period, an increase in diameters of the seminiferous tubules (up to 220 µm), and a proliferation of spermatogenic cells is observed [1]. On the other hand, at the end of the reproductive season, spermatogenesis is inactivated with seminiferous tubules that decrease in diameter up to 90 µm and lower cell density; at this stage, spermatogonia and Sertoli cells represent the only epithelial cellular components of the testis [7]. These cycling reproductive patterns are strictly related to blood and intra-testicular levels of steroid hormones, in particular testosterone (TEST): high levels are indeed necessary for successful spermatogenesis, good functionality of accessory sex glands, and mating outcome [1]. In bucks, TEST reaches its intra-testicular [6] and peripheral blood [8] peaks during the rut period, and decreases to basal levels starting from October [5]. The same trend applies to other sexual steroids including progesterone, androstenedione, and estradiol [8]. Another important steroid hormone is cortisol (CORT), generally used as stress marker for wildlife animals alongside corticosterone [9], since stress can impair reproductive efficiency and performances. One of the biggest limitations to hematic CORT quantification lies in the ultra-fast activation of the hypothalamic-pituitary-adrenocortical (HPA) system during stressful events [10], making it almost useless when assessing environmental chronic stressors. This is the reason why in the last decades, alternative biological matrices for CORT and other stress-related hormones quantification were investigated, including hair and feces [11,12]. Amongst the others, hair proved to be one of the best, if not the best, matrix to gain information regarding chronic and environmental stressors in different mammalian species [13–17], including humans [18]. Indeed, it is relatively easy and non-invasive to collect and less subject to deterioration [19]. Regarding the roe deer, alternative matrices such as feces were used to assess CORT concentrations [20], but hair, to the best of the authors’ knowledge, has never been taken into account. In the light of the cycling reproductive pattern of this species and its strong relationship with the environment, the evaluation of hair steroid hormones may provide interesting insights to further characterize this process. Therefore, the aim of the present work was to quantify hair concentrations of testosterone and cortisol in wild roe deer bucks hunted during either pre- or post-rut period, and to compare the results. The secondary objective was the evaluation of any possible correlations of such hair concentrations with blood and morphometric parameters of the testes. 2. Materials and Methods 2.1. Animals and Sampling Twenty-eight sexually mature roe deer bucks, 1 to 7 years old with body weights between 20.0 and 31.4 kg, were sampled during the 2017 hunting season between 1 June and 15 July (pre-rut, n = 14) and 15 August and 30 September (post-rut, n = 14). Animals were hunted in the South-Western Bologna Apennines (Italy) according to the regional hunting plan (Resolution No. 473 of the Emilia Romagna Regional Executive, 10 April 2017). Upon death, all the animals were immediately transferred to the pertinent biometrical center. Animals found dead within the territory during the hunting periods Animals 2018, 8, 113 3 of 9 were not included in the study to avoid biases related to possible pathological conditions. Ages were assessed upon analyses of teeth eruption and wear patterns. Upon arrival, the personnel of the centers collected blood from the jugular vein in sterile Lithium-heparin tubes, hair from the dorsal-caudal region and scrotums, including testes and epididymis. The samples were refrigerated (5 ± 1 ◦C) and transferred, using a cooler to maintain temperature, within 24 h to the physiology laboratories (ANFI-ASA) of the Department of Veterinary Medical Sciences of the University of Bologna (Ozzano dell’Emilia, Italy) [6]. Blood was centrifuged for 15 min at 1500× g to separate plasma which was divided into aliquots and stored at −20 ± 2 ◦C. It was previously demonstrated how steroids are stable in whole blood if kept refrigerated until centrifugation, which in the present case happened within 24 h [21,22]. Hair samples were stored at 5 ± 1 ◦C until analyses, while scrotums were immediately evaluated. Blood samples showing macroscopical alterations such as clots and scrotums damaged during collection were excluded from the study. Since all the biological specimens analyzed in this study were obtained from hunted animals (in accordance with the hunting plan in force), no ethical approval was necessary. 2.2. Testicular Analysis Testes were isolated from the scrotums and weighed using a lab scale (FCB 12K1, KERN & SOHN GmbH, Balingen, Germany) after epididymis ablation. For each animal, the weights of the two testes
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